Human activity is changing the global climate, and environmental stresses such as rising temperatures and heat waves are affecting many species. Biologists want to understand how different organisms cope with these changes: whether individuals can adjust their physiology to withstand stressful environments (a process known as acclimation), and whether populations can evolve over many generations to thrive in these changing environments (a process known as adaptation).
Two biological factors that could affect acclimation and adaptation are the epigenome and transposable elements (TEs). The epigenome consists of molecular changes to the structure and expression of the genome (the genome being the entire ensemble of an organism’s genes which is found in all nucleated cells), while TEs are fragments of genomic DNA that can replicate independently and insert themselves into new locations, giving natural selection new genetic variation to act on. These two factors interact: new TE insertions can influence gene expression through interactions with the epigenome, and both epigenomic change and TE activity are sensitive to environmental stresses such as heat shock. Understanding these interactions, and how they differ between populations, is therefore a key step in explaining how different organisms respond to global change.
Despite this, little is known about how interactions between environmental stress, the epigenome and transposable elements play out in natural populations. In the InterChromaTE project, I aimed to improve our understanding of these interactions and their potential evolutionary consequences. To do so, I measured natural population variation in TEs and a key epigenome trait, chromatin accessibility, which is linked to gene expression; I investigated whether differences influenced molecular and phenotypic responses to heat shock; and I explored whether heat stress responses could be transgenerationally inherited. To answer these questions, I used the fruit fly Drosophila, which due to its rapid life cycle and well-studied genome, made an ideal model organism.
My experiments showed that heat shock leads to clear changes in chromatin accessibility, gene expression and phenotype, and that these responses differ between populations. The relationship between chromatin accessibility and gene expression appeared to be influenced by the presence of TEs, an effect that also differed between populations. In one population, heat shock altered gene expression and phenotype not only in the stressed individuals, but in their great-grand offspring, highlighting an important transgenerational effect. Although chromatin accessibility did not seem to regulate this, it may be the result of an alternative epigenetic mechanism. Together, these results show the important role epigenome-TE interactions can play in the regulation of environmental stress responses, and how they have the potential to influence evolution through transgenerationally inherited phenotypes.
